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Checklist of Helminth Parasites of Goodeinae (Osteichthyes: Cyprinodontiformes: Goodeidae), an Endemic Subfamily of Freshwater Fishes from Mexico

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Checklist of Helminth Parasites of Goodeinae (Osteichthyes: Cyprinodontiformes: Goodeidae), an Endemic Subfamily of Freshwater Fishes from Mexico Zootaxa 3856 (2): 151–191 ISSN 1175-5326 (print edition) www.mapress.com/zootaxa/ Article ZOOTAXA Copyright © 2014 Magnolia Press ISSN 1175-5334 (online edition) http://dx.doi.org/10.11646/zootaxa.3856.2.1 http://zoobank.org/urn:lsid:zoobank.org:pub:F71F32F8-3CCE-4544-B36B-AC7EBBB676EF Checklist of helminth parasites of Goodeinae (Osteichthyes: Cyprinodontiformes: Goodeidae), an endemic subfamily of freshwater fishes from Mexico ANDRÉS MARTÍNEZ-AQUINO1, CARLOS A. MENDOZA-PALMERO2, ROGELIO AGUILAR-AGUILAR3 & GERARDO PÉREZ-PONCE DE LEÓN4,5 1División Zoología Invertebrados, Museo de La Plata, FCNyM, UNLP, Paseo del Bosque s/n, 1900 La Plata, Argentina. E-mail: [email protected] 2Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 370 05, České Budějovice, Czech Republic. E-mail: [email protected] 3Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México, C. P. 04510, México, D. F., Mexico. E-mail: [email protected] 4 Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Apartado Postal 70-153, C. P. 14510, México, D. F., Mexico. E-mail: [email protected] 5Corresponding author. E-mail: [email protected] Abstract From August 2008 to July 2010, 1,471 fish belonging to the subfamily Goodeinae (representing 28 species) were collected from 47 localities across central Mexico and analyzed for helminth parasites. In addition, a database with all available published accounts of the helminth parasite fauna of goodeines was assembled. Based on both sources of information, a checklist containing all the records was compiled as a necessary first step to address future questions in the areas of ecol- ogy, evolutionary biology and biogeography of this host-parasite association. The checklist is presented in two tables, a parasite-host list and a host-parasite list. The checklist contains 51 nominal species, from 34 genera and 26 families of helminth parasites. It includes 8 species of adult digeneans, 9 metacercarie, 6 monogeneans, 3 adult cestodes, 9 metaces- todes, 1 adult acanthocephalan, 1 cystacanth, 6 adult nematodes and 8 larval nematodes. Based on the amount of informa- tion contained in the checklist, we pose that goodeines, a subfamily of viviparous freshwater fishes endemic to central Mexico, might be regarded as the first group of wildlife vertebrate for which a complete inventory of their helminth par- asite fauna has been completed. Key words: taxonomy, Digenea, Monogenea, Cestoda, Nematoda, Acanthocephala, Mexico Introduction Freshwater fish helminth parasites are undoubtedly the best-known group among vertebrate parasites in Mexico (Pérez-Ponce de León & Choudhury 2010). The large number of published papers contributing to the inventory of the helminth parasite fauna of fish hosts, allowed Luque & Poulin (2007) to suggest that Mexico stands out as a hotspot of parasite diversity in freshwater fishes. The helminth parasite fauna of goodeines, a group of viviparous Cypronodontiform fishes, has been intensively studied in Mexico for the last three decades (Pérez-Ponce de León & Choudhury 2010; Garrido-Olvera et al. 2011). The entire subfamily Goodeinae is endemic to central and northern parts of Mexico (Domínguez-Domínguez et al. 2010). The inventory work of the helminth parasite fauna of this fish subfamily began with Lamothe-Argumedo (1970), who described the digenean Margotrema bravoae from the intestine of Girardinichthys multiradiatus in the Lerma River. However, it was not until the last 25 years that a series of studies was designed to survey the helminth fauna of this fish group. More than 50 studies have been published regarding some aspects of the helminth parasite fauna of goodeines, including descriptions of new species, local or regional inventories establishing new host and locality records, analyses of parasite community Accepted by A. Choudhury: 23 Jul. 2014; published: 22 Aug. 2014 151 both, Crenichthys Gilbert, which consists of two species, and Empetrichthys Miller, with four species, are endemic to Nevada, U.S., where small populations are found in isolated warm springs (Froese & Pauly 2013). This information is necessary to better understand the historical biogeography and evolutionary history of the helminth parasite fauna of this Nearctic freshwater fish group. Currently, interpretations are made regarding the phylogenetic and biogeographic relationships of goodeines with other members of the freshwater fish fauna in Mexico (see Pérez-Ponce de León and Choudhury, 2005; Pérez-Ponce de León et al. 2007; Martínez-Aquino et al. 2013). Also, helminth parasites of vertebrates have been used to track the evolutionary history of their hosts (Zietara & Lumme 2002; Nieberding et al. 2008; Laetsch et al. 2012). Therefore, information about parasites of Empetrichthyinae will represent the keystone to assess further questions about the evolutionary history of the host-parasite association in central and northern Mexico. Acknowledgments We thank R. Pérez-Rodríguez, D.I. Hernández-Mena, F.J. Alcántar-Escalera and L.H. Escalera-Vázquez for their help during field work. We are greateful with B. Mendoza-Garfías and L. Garrido-Olvera for processing some of the specimens, and L. García-Prieto for providing literature and specimens for morphological comparison deposited at the CNHE. Special thanks to O. Domínguez-Domínguez for earlier discussions of the findings of this manuscript. A.M-A. and C.A.M-P wishes to thank Consejo Nacional de Ciencia y Tecnología (CONACyT), Mexico for the scholarships granted to carry out their PhD studies (No. 202632, No. 192899, respectively). A.M-A. is currently supported by a postdoctoral grant from CONACYT (No. 207983). This study was supported by grants from the CONACyT (No. 83043) and Programa de Apoyo a Proyectos de Investigación e Innovación Tecnologíca (PAPIIT-UNAM IN202111 and 204514) to G.P.P.L. References Alcántar-Escalera, F.J., García-Varela, M., Vázquez-Domínguez, E. & Pérez-Ponce de León, G. (2013) Using DNA barcoding to link cystacanths and adults of the acanthocephalan Polymorphus brevis in central Mexico. Molecular Ecology Resources, 13, 1116–1124. http://dx.doi.org/10.1111/1755-0998.12090 Astudillo-Ramos, L. & Soto-Galera, E. (1997) Estudio helmintológico de Chirostoma humboldtianum y Girardinichthys multiradiatus capturados en el Lerma. Zoología Informa, 35, 53–59. Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al., revisited. Journal of Parasitology, 65, 667–669. http://dx.doi.org/10.2307/3284227 Caspeta-Mandujano, J.M. (2010) Nematode parasites of freshwater fish in Mexico. AGT Editor, México, 216 pp. Caspeta-Mandujano, J.M., Cabañas-Carranza, G. & Mendoza-Franco, E.F. (2009) Helmintos parásitos de peces dulceacuícolas mexicanos (Caso Morelos). AGT Editor, México, 129 pp. De la Vega-Salazar, M.Y. (2006) Estado de conservación de los peces de la familia Goodeidae (Cyprinodontiformes) en la mesa central de México. Revista de Biología Tropical, 54, 163–177. Domínguez-Domínguez, O., Mercado-Silva, N., Lyons, J. & Grier, H.J. (2005) The viviparous Goodeid fishes. In: Uribe, M.C. & Grier, H.J. (Eds.), Viviparous fishes. New Life Publications, Homestead, Florida, pp. 525–569. Domínguez-Domínguez, O., Pedraza-Lara, C., Gurrola-Sánchez, N., Pérez-Rodríguez, R., Israde-Alcántara, I., Garduño- Monroy, V.H., Doadrio, I., Pérez-Ponce de León, G. & Brooks, D.R. (2010) Historical biogeography of the Goodeinae (Cyprinodontiforms). In: Uribe-Aranzabal, M.C. & Grier, H.J. (Eds.), Viviparous Fishes II. New Life Publications, Homestead, Florida, pp. 33–74. Domínguez-Domínguez, O. & Pérez-Ponce de León, G. (2007) Los goodeidos, peces endémicos del centro de México. Biodiversitas, 75, 12–15. Ergens, R. (1969) The suitability of ammonium picrate-glycerin in preparing slides of lower monogenoidea. Folia Parasitologica, 16, 320. Froese, R. & Pauly, D. (Eds.) (2013) FishBase, World Wide Web electronic publication. Available from: www.fishbase.org (accessed 1 December 2013) García-Prieto, L., Mejía-Madrid, H. & Pérez-Ponce de León, G. (1988) Hallazgo del plerocercoide de Ligula intestinalis (Cestoda) en algunos peces dulceacuícolas de México. Anales del Instituto de Biología, Universidad Nacional Autónoma de México, Serie Zoología, 58, 887–888. García-Prieto, L. & Osorio-Sarabia, D. (1991) Distribución actual de Bothriocephalus acheilognathi en México. Anales del 188 · Zootaxa 3856 (2) © 2014 Magnolia Press MARTÍNEZ-AQUINO ET AL. Instituto de Biología, Universidad Nacional Autónoma de México, Serie Zoología, 62, 523–526. Garrido-Olvera, L., Arita, H.T. & Pérez-Ponce de León, G. (2012) The influence of host ecology and biogeography on the helminth species richness of freshwater fishes in Mexico. Parasitology, 12, 1652–1665. http://dx.doi.org/10.1017/S003118201200100X Guzmán-Cornejo, M.C. & García-Prieto, L. (1999) Trematodiasis en algunos peces del lago de Cuitzeo, Michoacán, México. Revista de Biología Tropical, 47, 593–596. Hoffman, G.L. (1999) Parasites of North American freshwater fishes. 2nd Edition. Cornell University Press, Ithaca, New York, 539 pp. Laetsch, D.R., Heitlinger, E.G., Taraschewski, H., Nadler S.A. & Blaxter, M.L. (2012) The phylogenetics of Anguillicolidae (Nematoda: Anguillicoloidea), swimbladder parasites of eels. BMC Evolutionary Biology, 12, 60. http://dx.doi.org/10.1186/1471-2148-12-60 Lamothe-Argumedo, R. (1970) Tremátodos de peces VI. Margotrema bravoae
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